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Title: Comparative genomics of a plant-parasitic nematode endosymbiont suggest a role in nutritional symbiosis

item BROWN, AMANDA - Oregon State University
item HOWE, D - Oregon State University
item WASALA, S - Oregon State University
item Peetz, Amy
item Phillips, Wendy
item Zasada, Inga
item DENVER, DEE - Oregon State University

Submitted to: Genome Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/30/2015
Publication Date: 9/10/2015
Citation: Brown, A.M., Howe, D.K., Wasala, S.K., Peetz, A.B., Phillips, W.S., Zasada, I.A., Denver, D.R. 2015. Comparative genomics of a plant-parasitic nematode endosymbiont suggest a role in nutritional symbiosis. Genome Biology and Evolution. 7:2727-2746.

Interpretive Summary: Plant-parasitic nematodes are microscopic roundworms that have been shown to cause significant yield loss to a range of crops. The focus of this research was the dagger nematode which can cause direct damage to plants and also transmit plant viruses to crops such as grapes, raspberries, and blueberries. The DNA from a population of dagger nematode was extracted and sequenced to explore the microbiome of this nematode. The bacteria Xiphinematobacter was found associated with the dagger nematode and the role that this bacterium plays in the nematode was explored using microscopy and by assembling the genome of the bacteria. It was discovered that this bacteria had a reduced genome size but retained genes for the biosynthesis of essential amino acids, amino acids required for the nematode to survive. These results are significant because they suggest that the bacteria supplement essential nutrients that are required in the nematode diet. This research will be used by scientists to develop novel targets, potentially the bacteria, to control the dagger nematode.

Technical Abstract: Bacterial mutualists can increase the biochemical capacity of animals. Highly co-evolved nutritional mutualists do this by synthesizing nutrients missing from the host's diet. Genomics tools have recently advanced the study of these partnerships. Here we examined the endosymbiont Xiphinematobacter (phylum Verrucomicrobia) from the dagger nematode Xiphinema americanum, a migratory ectoparasite of numerous crops that also vectors nepovirus. Previously, this endosymbiont was identified in the gut, ovaries and eggs, but its role was unknown. We explored the potential role of this symbiont using fluorescence in situ hybridization (FISH) microscopy, genome sequencing, and comparative functional genomics. Our study is novel in reporting the first genome from a non-Wolbachia nematode endosymbiont and an intracellular Verrucomicrobium. Results revealed Xiphinematobacter had a small ~0.916 Mbp genome with only 817 predicted proteins, resembling genomes of other mutualist endosymbionts. Compared with free-living relatives, conserved proteins were shorter on average, and there was large scale loss of regulatory pathways. Despite massive gene loss, genes for biosynthesis of essential amino acids were retained more than those for non-essential amino acids. Gene ontology (GO) enrichment tests showed enrichment for biosynthesis of arginine, tyrosine, histidine, aromatic amino acids, thiamine, and coenzyme A, whereas relatives Akkermansia muciniphilia (in the human colon), Methylacidiphilum infernorum and the mutualist Wolbachia from filarial nematodes showed different profiles. Together, these features and the location in the gut suggest Xiphinematobacter functions as a nutritional mutualist, supplementing essential nutrients that are depleted in the nematode diet. This pattern points to evolutionary convergence with endosymbionts found in sap-feeding insects.